Body-size shifts in aquatic and terrestrial urban communities.

Body size is intrinsically linked to metabolic rate and life-history traits, and is a crucial determinant of food webs and community dynamics1,2. The increased temperatures associated with the urban-heat-island effect result in increased metabolic costs and are expected to drive shifts to smaller body sizes 3 . Urban environments are, however, also characterized by substantial habitat fragmentation 4 , which favours mobile species. Here, using a replicated, spatially nested sampling design across ten animal taxonomic groups, we show that urban communities generally consist of smaller species. In addition, although we show urban warming for three habitat types and associated reduced community-weighted mean body sizes for four taxa, three taxa display a shift to larger species along the urbanization gradients. Our results show that the general trend towards smaller-sized species is overruled by filtering for larger species when there is positive covariation between size and dispersal, a process that can mitigate the low connectivity of ecological resources in urban settings 5 . We thus demonstrate that the urban-heat-island effect and urban habitat fragmentation are associated with contrasting community-level shifts in body size that critically depend on the association between body size and dispersal. Because body size determines the structure and dynamics of ecological networks 1 , such shifts may affect urban ecosystem function.

Evolution at two time frames: Polymorphisms from an ancient singular divergence event fuel contemporary parallel evolution.

When environments change, populations may adapt surprisingly fast, repeatedly and even at microgeographic scales. There is increasing evidence that such cases of rapid parallel evolution are fueled by standing genetic variation, but the source of this genetic variation remains poorly understood. In the saltmarsh beetle Pogonus chalceus, short-winged 'tidal' and long-winged 'seasonal' ecotypes have diverged in response to contrasting hydrological regimes and can be repeatedly found along the Atlantic European coast. By analyzing genomic variation across the beetles' distribution, we reveal that alleles selected in the tidal ecotype are spread across the genome and evolved during a singular and, likely, geographically isolated divergence event, within the last 190 Kya. Due to subsequent admixture, the ancient and differentially selected alleles are currently polymorphic in most populations across its range, which could potentially allow for the fast evolution of one ecotype from a small number of random individuals, as low as 5 to 15, from a population of the other ecotype. Our results suggest that cases of fast parallel ecological divergence can be the result of evolution at two different time frames: divergence in the past, followed by repeated selection on the same divergently evolved alleles after admixture. These findings highlight the importance of an ancient and, likely, allopatric divergence event for driving the rate and direction of contemporary fast evolution under gene flow. This mechanism is potentially driven by periods of geographic isolation imposed by large-scale environmental changes such as glacial cycles.

Evidence for Faster X Chromosome Evolution in Spiders.

In species with chromosomal sex determination, X chromosomes are predicted to evolve faster than autosomes because of positive selection on recessive alleles or weak purifying selection. We investigated X chromosome evolution in Stegodyphus spiders that differ in mating system, sex ratio, and population dynamics. We assigned scaffolds to X chromosomes and autosomes using a novel method based on flow cytometry of sperm cells and reduced representation sequencing. We estimated coding substitution patterns (dN/dS) in a subsocial outcrossing species (S. africanus) and its social inbreeding and female-biased sister species (S. mimosarum), and found evidence for faster-X evolution in both species. X chromosome-to-autosome diversity (piX/piA) ratios were estimated in multiple populations. The average piX/piA estimates of S. africanus (0.57 [95% CI: 0.55-0.60]) was lower than the neutral expectation of 0.75, consistent with more hitchhiking events on X-linked loci and/or a lower X chromosome mutation rate, and we provide evidence in support of both. The social species S. mimosarum has a significantly higher piX/piA ratio (0.72 [95% CI: 0.65-0.79]) in agreement with its female-biased sex ratio. Stegodyphus mimosarum also have different piX/piA estimates among populations, which we interpret as evidence for recurrent founder events. Simulations show that recurrent founder events are expected to decrease the piX/piA estimates in S. mimosarum, thus underestimating the true effect of female-biased sex ratios. Finally, we found lower synonymous divergence on X chromosomes in both species, and the male-to-female substitution ratio to be higher than 1, indicating a higher mutation rate in males.

Urbanization drives cross-taxon declines in abundance and diversity at multiple spatial scales.

The increasing urbanization process is hypothesized to drastically alter (semi-)natural environments with a concomitant major decline in species abundance and diversity. Yet, studies on this effect of urbanization, and the spatial scale at which it acts, are at present inconclusive due to the large heterogeneity in taxonomic groups and spatial scales at which this relationship has been investigated among studies. Comprehensive studies analysing this relationship across multiple animal groups and at multiple spatial scales are rare, hampering the assessment of how biodiversity generally responds to urbanization. We studied aquatic (cladocerans), limno-terrestrial (bdelloid rotifers) and terrestrial (butterflies, ground beetles, ground- and web spiders, macro-moths, orthopterans and snails) invertebrate groups using a hierarchical spatial design, wherein three local-scale (200 m × 200 m) urbanization levels were repeatedly sampled across three landscape-scale (3 km × 3 km) urbanization levels. We tested for local and landscape urbanization effects on abundance and species richness of each group, whereby total richness was partitioned into the average richness of local communities and the richness due to variation among local communities. Abundances of the terrestrial active dispersers declined in response to local urbanization, with reductions up to 85% for butterflies, while passive dispersers did not show any clear trend. Species richness also declined with increasing levels of urbanization, but responses were highly heterogeneous among the different groups with respect to the richness component and the spatial scale at which urbanization impacts richness. Depending on the group, species richness declined due to biotic homogenization and/or local species loss. This resulted in an overall decrease in total richness across groups in urban areas. These results provide strong support to the general negative impact of urbanization on abundance and species richness within habitat patches and highlight the importance of considering multiple spatial scales and taxa to assess the impacts of urbanization on biodiversity.

Male spiders control offspring sex ratio through greater production of female-determining sperm.

Sex allocation theory predicts that when sons and daughters have different reproductive values, parents should adjust offspring sex ratio towards the sex with the higher fitness return. Haplo-diploid species directly control offspring sex ratio, but species with chromosomal sex determination (CSD) were presumed to be constrained by Mendelian segregation. There is now increasing evidence that CSD species can adjust sex ratio strategically, but the underlying mechanism is not well understood. One hypothesis states that adaptive control is more likely to evolve in the heterogametic sex through a bias in gamete production. We investigated this hypothesis in males as the heterogametic sex in two social spider species that consistently show adaptive female-biased sex ratio and in one subsocial species that is characterized by equal sex ratio. We quantified the production of male (0) and female (X) determining sperm cells using flow cytometry, and show that males of social species produce significantly more X-carrying sperm than 0-sperm, on average 70%. This is consistent with the production of more daughters. Males of the subsocial species produced a significantly lower bias of 54% X-carrying sperm. We also investigated whether inter-genomic conflict between hosts and their endosymbionts may explain female bias. Next generation sequencing showed that five common genera of bacterial endosymbionts known to affect sex ratio are largely absent, ruling out that endosymbiont bacteria bias sex ratio in social spiders. Our study provides evidence for paternal control over sex allocation through biased gamete production as a mechanism by which the heterogametic sex in CSD species adaptively adjust offspring sex ratio.

Cross-taxa generalities in the relationship between population abundance and ambient temperatures.

Identifying patterns in the effects of temperature on species' population abundances could help develop a general framework for predicting the consequences of climate change across different communities and realms. We used long-term population time series data from terrestrial, freshwater, and marine species communities within central Europe to compare the effects of temperature on abundance across a broad range of taxonomic groups. We asked whether there was an average relationship between temperatures in different seasons and annual abundances of species in a community, and whether species attributes (temperature range of distribution, range size, habitat breadth, dispersal ability, body size, and lifespan) explained interspecific variation in the relationship between temperature and abundance. We found that, on average, warmer winter temperatures were associated with greater abundances in terrestrial communities (ground beetles, spiders, and birds) but not always in aquatic communities (freshwater and marine invertebrates and fish). The abundances of species with large geographical ranges, larger body sizes, and longer lifespans tended to be less related to temperature. Our results suggest that climate change may have, in general, positive effects on species' abundances within many terrestrial communities in central Europe while the effects are less predictable in aquatic communities.

Urbanization drives community shifts towards thermophilic and dispersive species at local and landscape scales.

The increasing conversion of agricultural and natural areas to human-dominated urban landscapes is predicted to lead to a major decline in biodiversity worldwide. Two conditions that typically differ between urban environments and the surrounding landscape are increased temperature, and high patch isolation and habitat turnover rates. However, the extent and spatial scale at which these altered conditions shape biotic communities through selection and/or filtering on species traits are currently poorly understood. We sampled carabid beetles at 81 sites in Belgium using a hierarchically nested sampling design wherein three local-scale (200 × 200 m) urbanization levels were repeatedly sampled across three landscape-scale (3 × 3 km) urbanization levels. First, we showed that communities sampled in the most urbanized locations and landscapes displayed a distinct species composition at both local and landscape scale. Second, we related community means of species-specific thermal preferences and dispersal capacity (based on European distribution and wing morphology, respectively) to the urbanization gradients. We showed that urban communities consisted on average of species with a preference for higher temperatures and with better dispersal capacities compared to rural communities. These shifts were caused by an increased number of species tolerating higher temperatures, a decreased richness of species with low thermal preference, and an almost complete depletion of species with very low-dispersal capacity in the most urbanized localities. Effects of urbanization were most clearly detected at the local scale, although more subtle effects could also be found at the scale of entire landscapes. Our results demonstrate that urbanization may fundamentally and consistently alter species composition by exerting a strong filtering effect on species dispersal characteristics and favouring replacement by warm-dwelling species.

Evolutionary history of a dispersal-associated locus across sympatric and allopatric divergent populations of a wing-polymorphic beetle across Atlantic Europe.

Studying the evolutionary history of trait divergence, in particular those related to dispersal capacity, is of major interest for the process of local adaptation and metapopulation dynamics. Here, we reconstruct the evolution of different alleles at the nuclear-encoded mitochondrial NADP(+)-dependent isocitrate dehydrogenase (mtIdh) locus of the ground beetle Pogonus chalceus that are differentially and repeatedly selected in short- and long-winged populations in response to different hydrological regimes at both allopatric and sympatric scales along the Atlantic European coasts. We sequenced 2788 bp of the mtIdh locus spanning a ~7-kb genome region and compared its variation with that of two supposedly neutral genes. mtIdh sequences show (i) monophyletic clustering of the short-winged associated mtIDH-DE haplotypes within the long-winged associated mtIDH-AB haplotypes, (ii) a more than tenfold lower haplotype diversity associated with the mtIDH-DE alleles compared to the mtIDH-AB alleles and (iii) a high number of fixed nucleotide differences between both mtIDH haplotype clusters. Coalescent simulations suggest that this observed sequence variation in the mtIdh locus is most consistent with a singular origin in a partially isolated subpopulation, followed by a relatively recent spread of the mtIDH-DE allele in short-winged populations along the Atlantic coast. These results demonstrate that even traits associated with decreased dispersal capacity can rapidly spread and that reuse of adaptive alleles plays an important role in the adaptive potential within this sympatric mosaic of P. chalceus populations.

Adaptation of a polyphagous herbivore to a novel host plant extensively shapes the transcriptome of herbivore and host.

Generalist arthropod herbivores rapidly adapt to a broad range of host plants. However, the extent of transcriptional reprogramming in the herbivore and its hosts associated with adaptation remains poorly understood. Using the spider mite Tetranychus urticae and tomato as models with available genomic resources, we investigated the reciprocal genomewide transcriptional changes in both spider mite and tomato as a consequence of mite's adaptation to tomato. We transferred a genetically diverse mite population from bean to tomato where triplicated populations were allowed to propagate for 30 generations. Evolving populations greatly increased their reproductive performance on tomato relative to their progenitors when reared under identical conditions, indicative of genetic adaptation. Analysis of transcriptional changes associated with mite adaptation to tomato revealed two main components. First, adaptation resulted in a set of mite genes that were constitutively downregulated, independently of the host. These genes were mostly of an unknown function. Second, adapted mites mounted an altered transcriptional response that had greater amplitude of changes when re-exposed to tomato, relative to nonadapted mites. This gene set was enriched in genes encoding detoxifying enzymes and xenobiotic transporters. Besides the direct effects on mite gene expression, adaptation also indirectly affected the tomato transcriptional responses, which were attenuated upon feeding of adapted mites, relative to the induced responses by nonadapted mite feeding. Thus, constitutive downregulation and increased transcriptional plasticity of genes in a herbivore may play a central role in adaptation to host plants, leading to both a higher detoxification potential and reduced production of plant defence compounds.

Persistent inter- and intraspecific gene exchange within a parallel radiation of caterpillar hunter beetles (Calosoma sp.) from the Galápagos.

When environmental gradients are repeated on different islands within an archipelago, similar selection pressures may act within each island, resulting in the repeated occurrence of ecologically similar species on each island. The evolution of ecotypes within such radiations may either result from dispersal, that is each ecotype evolved once and dispersed to different islands where it colonized its habitat, or through repeated and parallel speciation within each island. However, it remains poorly understood how gene flow during the divergence process may shape such patterns. In the Galápagos islands, three phenotypically similar species of the beetle genus Calosoma occur at higher elevations of different islands, while lowlands are occupied by a fourth species. By genotyping all major populations within this radiation for two nuclear and three mitochondrial gene fragments and seven microsatellite markers, we found strong support that the oldest divergence separates the highland species of the oldest island from the remaining species. Despite their morphological distinctness, highland species of the remaining islands were genetically closely related to the lowland population on each island and within the same magnitude as lowland populations sampled at different islands. Repeated evolution of highland ecotypes out of the lowland species appears the most likely scenario and estimates of geneflow rates revealed extensive admixture among ecotypes within islands, as well as between islands. These findings indicate that gene exchange among the different populations and species may have shaped the phylogenetic relationships and the repeated evolution of these ecotypes.

Inter and intra island introgression in a wolf spider radiation from the Galápagos, and its implications for parallel evolution.

Parallel radiations within island systems are often assumed to follow a simple scenario in which single colonization events are followed by in situ adaptive divergence. However, subsequent gene exchange after the initial colonization and during the divergence process might have important evolutionary impacts on species radiations. Gene exchange among ecologically similar species from different islands may lead to introgression of adaptive genetic variation and influence the parallel divergence process. In this study, we estimate levels of gene exchange within a wolf spider radiation of the genus Hogna Simon, 1885, from the Galápagos, wherein habitat specialization into 'high elevation' and 'coastal dry' species apparently evolved repeatedly on two islands. By using a multilocus approach we show that low levels of inter-island and relatively higher levels of intra island introgression shaped genetic variation in this species complex. Using these estimates, we demonstrate by means of a coalescence simulation that under these inter- and intra-island migration rates parallel evolution most likely evolves by introgression of adaptive alleles among islands, rather than through independent mutations despite the close genetic relationship of species within islands. As species phylogenies within radiations are frequently used to infer the divergence pattern, even relatively low levels of interspecific gene flow should not be neglected when interpreting parallel trait evolution.

A tight association in two genetically unlinked dispersal related traits in sympatric and allopatric salt marsh beetle populations.

Local adaptation likely involves selection on multiple, genetically unlinked traits to increase fitness in divergent habitats. Conversely, recombination is expected to counteract local adaptation under gene flow by breaking down adaptive gene combinations. Western European populations of the salt marsh beetle Pogonus chalceus are characterized by large interpopulation variation at various geographical ranges in two traits related to dispersal ability, i.e. wing size and different allozymes of the mitochondrial NADP(+)-dependent isocitrate dehydrogenase (mtIdh) gene. In this study, we tested whether variation in wing length was as strongly genetically determined in locally adapted populations in a sympatric mosaic compared to allopatric populations, and if variation in mtIDH and wing size was genetically unlinked. We demonstrate that the genetic determination of wing size is very high (h (2) = 0.90) in sympatry and of comparable magnitude as geographically separated populations. Second, we show that, although frequencies of mtIDH allozymes are tightly associated with mean population wing size across Western European populations, the correlation is strongly reduced within some of the populations. These findings demonstrate that the divergence involves at least two traits under independent genetic control and that the genetically distinct ecotypes are retained at geographical distances with ample opportunity for gene flow.

The ants of the Galápagos Islands (Hymenoptera, Formicidae): a historical overview, checklist, and identification key.

The Galápagos ant fauna has long been understudied, with the last taxonomic summary being published almost a century ago. Here, a comprehensive and updated overview of the known ant species of the Galápagos Islands is provided with updated species distributions. The list is based on an extensive review of literature, the identification of more than 382,000 specimens deposited in different entomological collections, and recent expeditions to the islands. The ant fauna is composed of five subfamilies (Dolichoderinae, Dorylinae, Formicinae, Myrmicinae, and Ponerinae), 22 genera, 50 species, and 25 subspecies, although three species (Crematogastercrinosa Mayr, 1862, Camponotussenex (Smith, 1858), and Solenopsissaevissima (Smith, 1855)) are considered dubious records. Finally, an illustrated identification key of the species found in the archipelago is presented.

Chromosomal inversions from an initial ecotypic divergence drive a gradual repeated radiation of Galápagos beetles.

Island faunas exhibit some of the most iconic examples where similar forms repeatedly evolve within different islands. Yet, whether these deterministic evolutionary trajectories within islands are driven by an initial, singular divergence and the subsequent exchange of individuals and adaptive genetic variation between islands remains unclear. Here, we study a gradual, repeated evolution of low-dispersive highland ecotypes from a dispersive lowland ecotype of Calosoma beetles along the island progression of the Galápagos. We show that repeated highland adaptation involved selection on multiple shared alleles within extensive chromosomal inversions that originated from an initial adaptation event on the oldest island. These highland inversions first spread through dispersal of highland individuals. Subsequent admixture with the lowland ecotype resulted in polymorphic dispersive populations from which the highland populations evolved on the youngest islands. Our findings emphasize the significance of an ancient divergence in driving repeated evolution and highlight how a mixed contribution of inter-island colonization and within-island evolution can shape parallel species communities.

Ideal free distribution of fixed dispersal phenotypes in a wing dimorphic beetle in heterogeneous landscapes.

According to the ideal free distribution (IFD) theory, individuals that are able to perceive the quality of different patches in a landscape and disperse freely are expected to redistribute themselves proportionally to the carrying capacities of heterogeneous patches. Here, we argue that, when dispersal is unconditional and genetically fixed, a coalition of sedentary and dispersing phenotypes can attain an IFD under spatiotemporally uncorrelated variation in fitness. This not only leads to a stable polymorphism of both dispersal phenotypes, but also implies that the number of dispersing individuals should on average be equal among patches and determined by the carrying capacity of the smallest local populations in the landscape. Differences in carrying capacity among patches are thus only reflected by changes in the number of sedentary individuals. Individual-based simulations show that this mechanism can be generalized over a wide range of spatiotemporal conditions and dispersal strategies. Moreover, these expectations are in strong agreement with empirical data on the density of both dispersal phenotypes of the wing dimorphic ground beetle Pterostichus vernalis within and among 10 different landscapes. Hence, for the first time, these results demonstrate that this mechanism serves as a plausible alternative to the competition-colonization model to explain the spatial distribution of fixed dispersal phenotypes in heterogeneous landscapes. Understanding of the frequency distributions of individuals expressing discrete dispersal morphs moreover improves our predictive and management capabilities for a broad range of species, for which we currently typically rely on using mean dispersal rates.

Dispersal capacity underlies scale-dependent changes in species richness patterns under human disturbance.

Changes in the species richness of (meta-)communities emerge from changes in the relative species abundance distribution (SAD), the total density of individuals, and the amount of spatial aggregation of individuals from the same species. Yet, how human disturbance affects these underlying diversity components at different spatial scales and how this interacts with important species traits, like dispersal capacity, remain poorly understood. Using data of carabid beetle communities along a highly replicated urbanization gradient, we reveal that species richness in urban sites was reduced due to a decline in individual density as well as changes in the SAD at both small and large spatial scales. Changes in these components of species richness were linked to differential responses of groups of species that differ in dispersal capacity. The individual density effect on species richness was due to a drastic 90% reduction of low-dispersal individuals in more urban sites. Conversely, the decrease in species richness due to changes in the SAD at large (i.e., loss of species from the regional pool) and small (i.e., decreased evenness) spatial scales were driven by species with intermediate and high dispersal ability, respectively. These patterns coincide with the expected responses of these dispersal-type assemblages toward human disturbance, namely, (i) loss of low-dispersal species by local extinction processes, (ii) loss of higher-dispersal species from the regional species pool due to decreased habitat diversity, and (iii) dominance of a few highly dispersive species resulting in a decreased evenness. Our results demonstrate that dispersal capacity plays an essential role in determining scale-dependent changes in species richness patterns. Incorporating this information improves our mechanistic insight into how environmental change affects species diversity at different spatial scales, allowing us to better forecast how human disturbance will drive local and regional changes in biodiversity patterns.

One to host them all: genomics of the diverse bacterial endosymbionts of the spider Oedothorax gibbosus.

Bacterial endosymbionts of the groups Wolbachia, Cardinium and Rickettsiaceae are well known for their diverse effects on their arthropod hosts, ranging from mutualistic relationships to reproductive phenotypes. Here, we analysed a unique system in which the dwarf spider Oedothorax gibbosus is co-infected with up to five different endosymbionts affiliated with Wolbachia, 'Candidatus Tisiphia' (formerly Torix group Rickettsia), Cardinium and Rhabdochlamydia. Using short-read genome sequencing data, we show that the endosymbionts are heterogeneously distributed among O. gibbosus populations and are frequently found co-infecting spider individuals. To study this intricate host-endosymbiont system on a genome-resolved level, we used long-read sequencing to reconstruct closed genomes of the Wolbachia, 'Ca. Tisiphia' and Cardinium endosymbionts. We provide insights into the ecology and evolution of the endosymbionts and shed light on the interactions with their spider host. We detected high quantities of transposable elements in all endosymbiont genomes and provide evidence that ancestors of the Cardinium, 'Ca. Tisiphia' and Wolbachia endosymbionts have co-infected the same hosts in the past. Our findings contribute to broadening our knowledge about endosymbionts infecting one of the largest animal phyla on Earth and show the usefulness of transposable elements as an evolutionary 'contact-tracing' tool.

A Novel Widespread MITE Element in the Repeat-Rich Genome of the Cardinium Endosymbiont of the Spider Oedothorax gibbosus.

Free-living bacteria have evolved multiple times to become host-restricted endosymbionts. The transition from a free-living to a host-restricted lifestyle comes with a number of different genomic changes, including a massive loss of genes. In host-restricted endosymbionts, gene inactivation and genome reduction are facilitated by mobile genetic elements, mainly insertion sequences (ISs). ISs are small autonomous mobile elements, and one of, if not the most, abundant transposable elements in bacteria. Proliferation of ISs is common in some facultative endosymbionts, and is likely driven by the transmission bottlenecks, which increase the level of genetic drift. In this study, we present a manually curated genome annotation for a Cardinium endosymbiont of the dwarf spider Oedothorax gibbosus. Cardinium species are host-restricted endosymbionts that, similarly to ColbachiaWolbachia spp., include strains capable of manipulating host reproduction. Through the focus on mobile elements, the annotation revealed a rampant spread of ISs, extending earlier observations in other Cardinium genomes. We found that a large proportion of IS elements are pseudogenized, with many displaying evidence of recent inactivation. Most notably, we describe the lineage-specific emergence and spread of a novel IS-derived Miniature Inverted repeat Transposable Element (MITE), likely being actively maintained by intact copies of its parental IS982-family element. This study highlights the relevance of manual curation of these repeat-rich endosymbiont genomes for the discovery of novel MITEs, as well as the possible role these understudied elements might play in genome streamlining. IMPORTANCE Cardinium bacteria, a widespread symbiont lineage found across insects and nematodes, have been linked to reproductive manipulation of their hosts. However, the study of Cardinium has been hampered by the lack of comprehensive genomic resources. The high content of mobile genetic elements, namely, insertion sequences (ISs), has long complicated the analyses and proper annotations of these genomes. In this study, we present a manually curated annotation of the Cardinium symbiont of the spider Oedothorax gibbosus. Most notably, we describe a novel IS-like element found exclusively in this strain. We show that this mobile element likely evolved from a defective copy of its parental IS and then spread throughout the genome, contributing to the pseudogenization of several other mobile elements. We propose this element is likely being maintained by the intact copies of its parental IS element and that other similar elements in the genome could potentially follow this route.

A masculinizing supergene underlies an exaggerated male reproductive morph in a spider.

In many species, individuals can develop into strikingly different morphs, which are determined by a simple Mendelian locus. How selection shapes loci that control complex phenotypic differences remains poorly understood. In the spider Oedothorax gibbosus, males develop either into a 'hunched' morph with conspicuous head structures or as a fast-developing 'flat' morph with a female-like appearance. We show that the hunched-determining allele contains a unique genomic fragment of approximately 3 megabases that is absent in the flat-determining allele. This fragment comprises dozens of genes that duplicated from genes found at the same as well as different chromosomes. All functional duplicates, including a duplicate of the key sexual differentiation regulatory gene doublesex, show male-specific expression, which illustrates their integrated role as a masculinizing supergene. Our findings demonstrate how extensive indel polymorphisms and duplications of regulatory genes may contribute to the evolution of co-adapted gene clusters, sex-limited reproductive morphs and the enigmatic evolution of exaggerated sexual traits in general.

Ecology and evolution of chlamydial symbionts of arthropods.

The phylum Chlamydiae consists of obligate intracellular bacteria including major human pathogens and diverse environmental representatives. Here we investigated the Rhabdochlamydiaceae, which is predicted to be the largest and most diverse chlamydial family, with the few described members known to infect arthropod hosts. Using published 16 S rRNA gene sequence data we identified at least 388 genus-level lineages containing about 14 051 putative species within this family. We show that rhabdochlamydiae are mainly found in freshwater and soil environments, suggesting the existence of diverse, yet unknown hosts. Next, we used a comprehensive genome dataset including metagenome assembled genomes classified as members of the family Rhabdochlamydiaceae, and we added novel complete genome sequences of Rhabdochlamydia porcellionis infecting the woodlouse Porcellio scaber, and of 'Candidatus R. oedothoracis' associated with the linyphiid dwarf spider Oedothorax gibbosus. Comparative analysis of basic genome features and gene content with reference genomes of well-studied chlamydial families with known host ranges, namely Parachlamydiaceae (protist hosts) and Chlamydiaceae (human and other vertebrate hosts) suggested distinct niches for members of the Rhabdochlamydiaceae. We propose that members of the family represent intermediate stages of adaptation of chlamydiae from protists to vertebrate hosts. Within the genus Rhabdochlamydia, pronounced genome size reduction could be observed (1.49-1.93 Mb). The abundance and genomic distribution of transposases suggests transposable element expansion and subsequent gene inactivation as a mechanism of genome streamlining during adaptation to new hosts. This type of genome reduction has never been described before for any member of the phylum Chlamydiae. This study provides new insights into the molecular ecology, genomic diversity, and evolution of representatives of one of the most divergent chlamydial families.